About 30% of the production of citrus fruits (and 40% of orange production) is processed (USDA-FAS, 2010), principally to make juice, and results in large quantities of by-products. Citrus pulp is the solid residue that remains after fresh fruits are squeezed for their juice. It amounts to 50-70% of the fresh weight of the original fruit and contains the peel (60-65%), internal tissues (30-35%) and seeds (0-10%) (Crawshaw, 2004; Göhl, 1978). Citrus pulp is usually made from oranges but may also contain by-products of other citrus fruits, notably grapefruits and lemons (Crawshaw, 2004).

Citrus pulp is used as a cereal substitute in ruminant feeds, due to its high energy content and good digestibility in ruminant species. Fresh pulp is often used locally to feed animals. Fresh citrus pulp has a natural acidity but it is still a perishable product due to its high content of water and soluble sugars (Rihani, 1991). It may quickly sour, ferment and release sludge hazardous to the environment. It stores well in the absence of air and fresh pulp can be preserved by ensiling and alkali treatments such as ammoniation (see the Fresh citrus pulp datasheet for more information).

Dried citrus pulp is sometimes used as a poultry bedding material and mixtures of dried citrus pulp and poultry litter have been used as livestock feed (Göhl, 1978).

Distribution

Dried citrus pulp is available worldwide. In 2010, world production was below 2 million tons (Licht, 2010). The main producer of citrus fruit for processing is Brazil (47% of the production), followed by the USA (29%) (USDA-FAS, 2010).

Processes

During the drying process, the water content of citrus pulp decreases from about 80% to 11% water (Grant, 2007). The drying process requires the addition of lime (quicklime (CaO) or hydrated lime (Ca(OH)2)) to neutralize the free acids, bind the fruit pectins and release water (Wing, 2003; Göhl, 1978). The mixture of fresh pulp and lime is then pressed to remove the excess moisture. The resulting liquid, rich in soluble sugars, is concentrated to make citrus molasses that can be fed to animals, sold to distillers or reintroduced in the final pulp. Other components such as essential oils and limonenes can also be extracted (Rihani, 1991; Grant, 2007). Once the liquid is removed, the pressed pulp is dried in a natural gas dryer (some Brazilian companies use sugarcane bagasse as fuel for this operation) and then pelleted and cooled (European Union, 1999; Göhl, 1978; Grant, 2007). Over-heating during the pelleting process can cause charring, which may decrease the nutritional value (Arthington et al., 2002).

In areas where fuel costs are low, the fresh pulp can also be dried directly in a rotary drier. Such pulps have a higher sugar content (Göhl, 1978).

Environmental impact

Citrus juice production is often a highly integrated industry, and its environmental impact must be assessed across the entire production chain, from fruit cultivation to the production of juice and essential oils. Life-cycle assessments of the citrus industry have been made for Italy (Beccali et al., 2009; Beccali et al., 2010), Brazil (Coltro et al., 2009) and Spain (Ribal et al., 2009). Typically, citrus production requires irrigation, pesticides, herbicides, fertilizers and soil correctors. Fruit selection and washing, juice and essential oil production as well as citrus pulp dehydration all need fossil fuel energy and result in wastewaters that require treatment facilities.

The use of citrus pulp for animal feeding was found to be an effective way to decrease waste output. An exhaustive analysis should include an assessment of the environmental burdens associated to substitute feeds, and of the associated costs of other methods of citrus pulp disposal. Anaerobic digestion of citrus pulp can produce biogas to be used in the manufacturing process, thereby reducing the energy demand, but it does not reduce waste (Beccali et al., 2010).

Nutritional aspects

Nutritional attributes

Dried citrus pulp is considered as an energy concentrate feed and a cereal substitute for ruminants (Arthington et al., 2002). It has a high fibre content (about 20% NDF in DM) and contains large amounts (10-40% DM) of highly digestible peptic substances and water soluble sugars (mostly sucrose) (Rihani, 1991). It is also rich in calcium (1-2% DM), due to the lime added in the drying process, which may triple the original calcium content (Rihani, 1991; Crawshaw, 2004). Its protein content is low (about 5-10% DM) as are ether extract (about 2% DM) and phosphorus (about 0.1% DM). The nutritive value of dried citrus pulp is variable and depends on many factors, the main one being the relative proportion of skins and seeds, which, among other factors, varies according to the citrus species and variety, the harvesting process and season (Rihani, 1991). For example orange pulp contains typically more sucrose and protein and less NDF and lipids than pulps from lemons (Rihani, 1991; Crawshaw, 2004). Oranges and grapefruits harvested in October contain more seeds, and thus more protein and ether extract, than those harvested in April (Rihani, 1991). Citrus pulp with citrus molasses added has a higher sugar content and less fibre than citrus pulp without molasses, and the level of calcium is linked to the amount of added lime (Arthington et al., 2002; Rihani, 1991).

The high fibre content makes it essentially a feed for ruminants and animals that can easily digest fibre. It is much less valuable to pigs and poultry due to the fibre content and to the presence of limonin in the seeds, which is toxic to monogastrics (Göhl, 1982).

Mycotoxins

Due to its hygroscopic capacity, dried citrus pulp is susceptible to moulds, particularly in humid tropical climates. These moulds produce secondary metabolites such as aflatoxins and citrinin (the latter know to cause hemorrhagic syndrome) (Oliveira et al., 2004; Melo et al., 1999; Griffiths et al., 1991). Drying and pelleting should destroy the moulds and mycotoxicosis due to citrus pulp is uncommon, but a visual inspection before feeding is recommended (Arthington et al., 2002).

Limonin

Limonin is a triterpenoid present in the seeds and skins that imparts a bitter taste to citrus pulp. If large quantities of seeds are present their limonin content may render the pulp toxic to non-ruminants at inclusion rates as low as 2.5% of the diet (Rihani, 1991; Fuller, 2004; Devendra, 1988). It has been suggested that limonin caused intestinal irritation and poor absorption of the nutriments in broilers (El Boushy et al., 2000).

Limonin should not be confounded with limonene, another terpenoid present in large quantities in citrus peels and that is responsible for the characteristic odour of citrus. Limonene is practically non-toxic to birds and mammals (EPA, 1994).

Lectins

There have been reports of a Type IV hypersensitivity reaction that caused death from haemorrhage and heart failure of several cows fed citrus pulp. This inflammatory reaction may be the result of a lectin-like haemaglutinous activity thought to be present in citrus pulp. This condition could not be reproduced in sheep and rabbits (Saunders et al., 2000; Tokarnia et al., 2001).

Other natural compounds

Compounds such as tannins, saponins, phytates, oxalates and flavonoids have been identified in citrus peels but they are below the levels reported to be toxic to livestock species (Oluremi et al., 2007).

Pesticides

Contamination with pesticide residues can occur and depends on the compound used, dosage, rainfall at the time of application, time between applications, harvest method and citrus species. In Brazil, pesticide residues in citrus pulp have decreased in the early 2000s, due to a more rational application of pesticides (Oliveira et al., 2004).

Dioxin

In 1998, 100,000 tons of citrus pulp pellets from Brazil contaminated with dioxin were imported into Germany. The source of contamination with dioxin was found to be the lime used in the drying process (European Union, 1999; Malisch, 2000).

Ruminants

Dried citrus pulp is a common ingredient in ruminant diets and compound feeds throughout the world. In the tropics, it can enhance tropical beef and dairy production systems based on low to medium nutritive value grasses and other forage sources (Villareal et al., 2006).

Energy value and digestibility

Due to its relatively high digestibility (OMD in the 85-90% range) and energy value (ME about 2900 kcal/kg DM, 85-90% that of maize and comparable to barley ME), citrus pulp is used as a cereal substitute in concentrate diets (Bampidis et al., 2006; Villareal et al., 2006). Unlike cereals, its energy is not based on starch but on soluble carbohydrates and digestible fibre. Citrus pectins are easily and extensively degraded, producing acetic acid, which is less likely than lactic acid to cause a fall in pH resulting in acidosis (Wing, 2003). Due to its high fibre content, the long rumination of citrus pulp produces large quantities of saliva that has a buffering effect on rumen pH (Mertens, 2000; Faria et al., 2008). Citrus pulp is therefore considered as a safer feed than cereals for animals fed high-concentrate, low-roughage diets, such as high-yielding dairy cows (Crawshaw, 2004). In rations containing low digestibility forages (hay or straw) or based on roughages such as maize silage or sorghum silage, citrus pulp seems to have a positive effect on fibre digestibility, perhaps due to a longer rumen retention time (Arthington et al., 2002; Barrios-Urdaneta et al., 2003).

Supplementation

The digestibility of the protein of citrus pulp is low and variable (from 37% to 70%) and, therefore, including large amounts of citrus pulp in diets containing protein-rich forages may cause a general decrease in protein digestibility. Its low soluble nitrogen content may result in a decrease in rumen ammonia. Supplementation with urea or ammonia can be a valuable strategy. Citrus pulp contains highly fermentable carbohydrates that may promote a more efficient use of N, by increasing the production of microbial protein by the rumen bacteria (Rihani, 1991). However, true protein sources can be more efficient than non-protein N (Kim et al., 2007).

Due to the low phosphorus content and to the Ca:P imbalance, phosphorus supplementation is an important consideration for balanced diets containing citrus pulp (Arthington et al., 2002).

As citrus pulp has a low content of vitamin A, green leafy roughage is an important ingredient in rations with high levels of citrus pulp (Göhl, 1982).

Palatability

The palatability of dried citrus pulp is variable, as it may have a bitter taste due to limonin and other compounds present in the seeds and peels. It can result in a decrease in intake if introduced too quickly in the diet, and a more progressive introduction is recommended. It is well accepted by animals that are accustomed to it and can then increase intake (Rihani, 1991; Wing, 2003; Göhl, 1978). In fattening lambs, palatability decreased when diets contained more than 40% dried citrus pulp (Bhattacharya et al., 1973).

Cattle

Dairy cattle

Citrus pulp is a valuable feedstuff for dairy cows. The extensive acetic acid production in the rumen helps maintain milk yield and milk fat content when forage is scarce (low fibre diet) or when high energy is required (e.g. as a replacement for cereals) (Arthington et al., 2002). A comprehensive review of past literature indicates that dried citrus pulp has no useful dietary properties other than its nutrient content, which limits its use in dairy cattle concentrate rations (Wing, 2003). It is not a full substitute for cereals and while it does have roughage-sparing properties, it cannot be used in place of the entire roughage allowance (Wing, 2003; Crawshaw, 2004).

Early research reported that citrus pulp could cause milk taint under certain conditions, but this has not been confirmed experimentally (Crawshaw, 2004).

Beef cattle and growing cattle

Dried citrus pulp is also a valuable feed for beef and growing cattle and can partly replace cereal energy sources. It can be safely included in rations at 20-30% of the DM (Crawshaw, 2004), but higher values are feasible. It was possible to include up to 40% dried citrus pulp in the diet of fattening cattle without altering animal health (Oliveira et al., 2002; Oliveira et al., 2005). Up to 55% dried pulp in the diets of young bulls (replacing 86% of maize grain) did not affect live-weight gain and carcass yield, though there was a decrease in backfat thickness (Henrique et al., 2004; Henrique et al., 2006). In beef cattle fed low-quality star grass (Cynodon nlemfuensis), increasing the amounts of dried citrus pulp up to 2.5 kg/day/animal (as fed), equal to 30% of the diet DM, reduced forage intake but increased energy intake (Villareal et al., 2006). Urinary calculi have been observed in steers fattened with rations of more than 30% citrus meal (Göhl, 1978).

Citrus pulp at 30% of the diet is acceptable in rations for calves over two months old, but it is not recommended for younger calves because of depressed intake (Wing, 2003). A 45% inclusion rate in calf rations was also reported (Göhl, 1978).

Ewes

Inclusion of 30% citrus pulp in the concentrate given to lactating ewes fed alfalfa hay and straw did not affect milk yield and milk composition (Fegeros et al., 1995). Another experiment reported that replacing 33% to 100% of barley with citrus pulp in diets based on ammoniated straw resulted in a linear decrease in milk yield, but not milk composition, and a lower daily weight gain of lambs (Castrillo et al., 2004).

Goats

In male goats, supplementation with dried citrus (lemon) pulp and urea of a diet based on barley straw and alfalfa hay increased DM intake and apparent dry matter digestibility of the straw (Madrid et al., 1997). However, a later experiment showed that digestibility decreased when a supplement of 300 g/day/animal was given (Madrid et al., 1998). In growing kids, replacing maize grain with 40% citrus pulp gave the best daily weight gain, DM intake and feed conversion while higher levels were thought to have deleterious effects on mineral metabolism (Bueno et al., 2002).

Dry citrus pulp can also be incorporated into goat rations as a dry season supplement to foliage from leguminous browse plants (Enterolobium cyclocarpum), replacing up to 50% of the concentrate (dried brewer's grains) (Oni et al., 2008).

Pigs

Citrus pulp is bulky and more fibrous than cereals and therefore less valuable in pigs than in ruminants. The presence of limonin-containing pips may be a limiting factor and citrus pulps from seedless fruits could be more usable than pulps containing seeds (Crawshaw, 2004). Sows seem to be more able to digest citrus pulp than growing pigs.

Growing pigs

Dried citrus pulp may be included at up to 5% in the diet of growing pigs (O'Sullivan et al., 2003). Higher rates can adversely affect growth rates (O'Sullivan et al., 2003; Baird et al., 1974), feed conversion efficiency and carcass yield (O'Sullivan et al., 2003). However, another experiment reported that up to 15% citrus pulp had no unfavourable effects on digestibility and energy value provided that phosphorus and vitamin D were added (Nicolakakis et al., 1999). In many case, serious health problems (anorexia, locomotion problems, hyperthermia, erythema) have been reported at a 15% inclusion rate (Santos et al., 2002) suggesting caution should be exercised when rates higher than 10% are used.

Sows

Dried citrus pulp may be included at up to 20% and 15% in the diets of pregnant and lactating sows respectively, without affecting reproductive performance, sow body weight, piglet weight at birth or at weaning and voluntary feed intake (O'Sullivan et al., 2003). Another experiment reported using up to 50% citrus pulp in gestating and lactating sows without deleterious effects on performances and productive indices (Sotto et al., 2009).

Poultry

Dried citrus pulp, even at low levels, has not proved useful in poultry diets.

Broilers

Levels between 5% and 10% of citrus pulp in the diet increased soluble non-starch polysaccharides and led to impaired growth rates, lower feed efficiency and reduced carcass yields. The 10% level changed fatty acid profile of the meat, depressing monounsaturated fatty acids and palmitic acid and increasing the predominance of n-6 and n-3 polyunsaturated fatty acids (Mourao et al., 2008). Dried citrus peels improved final live weight and live-weight gain up to 7.5% inclusion, and reduced serum cholesterol concentration (Chaudry et al., 2004). Sun-dried sweet orange rinds collected from retailers of peeled oranges could be used to replace up to 15-20% maize (about 7-9% of the total diet) in the diet of broilers without any adverse effect on performance (Oluremi et al., 2006; Agu et al., 2010). A summary of earlier experiments reported the 7.5% inclusion rate in the diet as the most favourable (El Boushy et al., 2000).

Laying hens

A 5% inclusion rate seems to be safe in laying hens (El Boushy et al., 2000), but higher rates have been suggested. 10% dried citrus peel in the diet of laying hens had no significantly adverse effect on feed intake, egg production, and egg weight (Yang et al. 1985). A level of 12% dried citrus pulp in the diet did not affect performance and egg quality of laying hens in the early stage of production (Nazok et al., 2010). A diet with 15% citrus peels decreased feed efficiency and gave darker egg yolks (Yang et al. 1985).

Quails

Using up to 6% dried citrus pulp in diets for laying quails had no significantly adverse effects on performance (Florou-Paneri et al., 2001).

Rabbits fed citrus pulp (up to 51.5 g/day), similar to that had caused severe health issues in cattle, did not show signs of poisoning or other symptoms (Tokarnia et al., 2001).

Horses and donkeys

In an experiment with crossbred horses (492 kg), citrus pulp could be used in horse diets at up to 28% concentrate. Citrus pulp was found to be a safe energy source that benefits the digestibility of the nutrients and the carbohydrate fraction (both the fibrous and non-fibrous fractions) of the diet. (Brandi et al., 2014).

Fish

Use of dried citrus pulp as part as fish diets has been reported in several fish species: